In addition to showing how to identify a group-level adaptation (see part I), George Williams also made a strong empirical claim: Individual-level selection is almost invariably stronger than group-level selection. Putting his empirical claim together with his principle, he concluded that “group-related adaptations do not, in fact exist” (Adaptation and Natural Selection p. 93). In the lemming example, the group-level advantage of conserving resources is just too weak to counter the individual-level disadvantage of committing suicide. If lemmings actually do run off cliffs into the sea (as opposed to being thrown off by the crew of the Disney movie that made the example famous) then it will need to be explained another way, not as a group-level adaptation. George made this claim not only for the lemming example, but for virtually all putative examples of group-level selection.
Before continuing, I want to acknowledge that if George’s empirical claim did turn out to be correct, it would be a very strong argument for individualism, which is the claim that adaptations exist only at the individual level; that individuals are the only units that can be called self-interested; that a group cannot be described as an organism writ large. All of these statements would be true if natural selection operated entirely at the individual level according to Williams’ principle.

But it’s not true, and the legacy of George Williams can be used to prove my point. In addition to the fanciful lemming example, George was on the lookout for other traits that could be used to test the relative strengths of individual and group selection, including sex ratio, or the proportion of sons and daughters among one’s offspring. Elliott and I discuss this example in detail in our book Unto Others, but it is worth repeating here for a general audience to show how a seemingly arcane trait such as sex ratio can play an important role in evolutionary thought for it’s ability to shed light on a foundational issue such as levels of adaptation.

The sex ratio of one’s offspring is not as dramatic as suicide, but it too has consequences for natural selection within and among groups. The logic is a bit complex, but trust me that natural selection within groups favors an equal proportion of sons and daughters, or an equal investment to be more precise, as Ronald Fisher first established in the 1930’s. George observed that the consequences of sex ratio at the group level depended on some details. If food was plentiful and the population was growing, then populations with a female-biased sex ratio would grow faster; after all, it is females who have the offspring. If food was short and the population needed to conserve resources, then a male-biased sex ratio would reduce population size in the same way as suicide. Either way, an even sex ratio signifies that individual-level selection plays a much more important role than group-level selection in the evolution of sex ratios.

George was unaware of examples of biased sex ratios at the time and regarded even sex ratios as the strongest evidence for his more general empirical claim that “group-level adaptations do not, in fact exist.” Today we know that sex ratios are biased in thousands of species and that many examples count as evidence for group selection when Williams’ principle is carefully applied to them. In other words the biased sex ratios are indeed selectively disadvantageous within groups but nevertheless evolve on the strength of causing the group to differentially contribute to the total population. George had the integrity to change his mind about sex ratio, writing in his 1992 book Natural Selection: Domains, Levels and Challenges (p. 49) that “I think it is desirable…to realize that selection in female-biased Mendelian populations favors males, and that it is only the selection among such groups that can favor the female bias.”

George retracted his own empirical claim a second time when he became interested in Darwinian medicine, one of his other great contributions to evolutionary thought. Disease organisms are ideal for studying multilevel selection because individuals are so clearly nested within groups (=hosts). The traits that are maximally adaptive within a host, such as replicating as fast as possible, are usually not the same as the traits that maximize the transmission of the group of disease organisms as a whole to other hosts. After reviewing the evidence, George concluded in an article written with Randy Nesse (see p. 51 of Unto Others for details) that “this is a clear example of group vs. individual (clone) selection for altruism, for which many formal models have been proposed.”

I will provide one other empirical example of group selection because it is so close to the lemming example. In a clever experiment, a group of scientists headed by Benjamin Kerr examined the evolution of virulence in viral phages that prey upon the bacteria E. Coli. The groups were the wells of multi-well plates used for chemical analysis and dispersal among groups was accomplished by automated pipettes. Phage strains differed in their virulence and the most virulent strains outcompeted the less virulent strains within each well. However, the most virulent strains also drove their prey and themselves extinct, leaving those wells available for colonization by groups containing less virulent strains. If that’s not an example of group selection according to Williams’ principle, what would be?

Not only can dozens of other empirical examples be cited, but group selection is no longer contested on theoretical grounds. When George wrote Adaptation and Natural Selection in the 1960’s, it seemed hard to construct a theoretical model that showed how group selection could successfully oppose individual selection. Starting in the 1970’s, models by George Price, Michel Ghiselin, and myself showed that group selection can be a significant evolutionary force after all. The fascinating story of George Price is told by historian Oren Solomon Harman in his recent book titled The Price of Altruism.

Thus, if by individualism we mean “individual selection invariably trumps group selection according to Williams’ principle”, then it is dead. As University of Oxford evolutionist Andy Gardner put it in a commentary on group selection published in Nature, “Everyone agrees that group selection occurs”. The only way that individualism has managed to survive is by transmuting, virus-like, to another form.